Bupropion binds to two sites in the Torpedo nicotinic acetylcholine receptor transmembrane domain: A photoaffinity labeling study with the bupropion analogue [ 125I]-SADU-3-72

Biochemistry

Volumn 51, Issue 12, 2012, Pages 2425-2435

  Pandhare, Akash ^a   Hamouda, Ayman K ^b   Staggs, Brandon ^a   Aggarwal, Shaili ^c   Duddempudi, Phaneendra K ^a   Lever, John R ^d,e   Lapinsky, David J ^c   Jansen, Michaela ^a   Cohen, Jonathan B ^b   Blanton, Michael P ^a  

^a TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER SCHOOL OF MEDICINE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c DUQUESNE UNIVERSITY   (United States)

^d UNIVERSITY OF MISSOURI   (United States)

^e VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING POCKETS; BUPROPION; DESENSITIZED STATE; EXTRACELLULAR; HIGH AFFINITY; HIGH-AFFINITY SITES; INGEL DIGESTION; ION CHANNEL; ION CHANNEL BLOCKERS; NICOTINIC ACETYLCHOLINE RECEPTORS; NICOTINIC ACETYLCHOLINE RECEPTORS (NACHRS); PHOTOAFFINITY LABELING; PHOTOINCORPORATION; PHOTOLABELING; RESTING STATE; TETRACAINE; TRANS-MEMBRANE DOMAINS;

ACTIVATION ANALYSIS; AMINO ACIDS; ANESTHETICS; BINDING SITES; IONS; TOBACCO;

TORPEDOES;

2 (N TERT BUTYLAMINO) 3' IODO 4' AZIDOPROPIOPHENONE I 125; AMFEBUTAMONE; CHEMICAL COMPOUND; LEUCINE; METHIONINE; NICOTINIC RECEPTOR; NICOTINIC RECEPTOR BETA; NICOTINIC RECEPTOR DELTA; NICOTINIC RECEPTOR GAMMA; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; DOSE RESPONSE; DRUG PROTEIN BINDING; FEMALE; IC 50; NONHUMAN; PHOTOAFFINITY LABELING; PRIORITY JOURNAL; PROTEIN DOMAIN; TORPEDO CALIFORNICA;

ANIMALS; ANTIDEPRESSIVE AGENTS; AZIDES; BINDING SITES; BUPROPION; CELL MEMBRANE; NICOTINIC ANTAGONISTS; PHOTOAFFINITY LABELS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, NICOTINIC; TORPEDO;

EID: 84859186479     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi300101r     Document Type: Article

References (40)

1. Wilkes, S. (2008) The use of bupropion SR in cigarette smoking cessation Int. J. Chron. Obstruct. Pulmon. Dis. 3, 45-53
2. Fryer, J. D. and Lukas, R. J. (1999) Noncompetitive functional inhibition at diverse, human nicotinic acetylcholine receptor subtypes by bupropion, phencyclidine, and ibogaine J. Pharmacol. Exp. Ther. 288, 88-92
3. Slemmer, J. E., Martin, B. R., and Damaj, M. I. (2000) Bupropion is a nicotinic antagonist J. Pharmacol. Exp. Ther. 295, 321-327
4. Carroll, F. I., Blough, B. E., Mascarella, S. W., Navarro, H. A., Eaton, J. B., Lukas, R. J., and Damaj, M. I. (2010) Synthesis and biological evaluation of bupropion analogues as potential pharmacotherapies for smoking cessation J. Med. Chem. 53, 2204-2214
5. Arias, H. R. (2010) Molecular interaction of bupropion with nicotine acetylcholine receptors J. Pediatr. Biochem. 1, 185-197
6. Thompson, A. J., Lester, H. A., and Lummis, S. C. (2010) The structural basis of function in Cys-loop receptors Q. Rev. Biophys. 43, 449-499
7. Bouzat, C. New insights into the structural bases of activation of Cys-loop receptors. J. Physiol. (Paris) 2011, not supplied.
8. Unwin, N. (2005) Refined structure of the nicotinic acetylcholine receptor at 4A resolution J. Mol. Biol. 346, 967-989
9. De Biasi, M. and Dani, J. A. (2011) Reward, addiction, withdrawal to nicotine Annu. Rev. Neurosci. 34, 105-130
10. Dani, J. A. and Bertrand, D. (2007) Nicotinic acetylcholine receptors and nicotinic cholinergic mechanisms of the central nervous system Annu. Rev. Pharmacol. Toxicol. 47, 699-729
11. Arias, H. R., Gumilar, F., Rosenberg, A., Targowska-Duda, K. M., Feuerbach, D., Jozwiak, K., Moaddel, R., Wainer, I. W., and Bouzat, C. (2009) Interaction of bupropion with muscle-type nicotinic acetylcholine receptors in different conformational states Biochemistry 48, 4506-4518
12. Lapinsky, D. J., Aggarwal, S., Nolan, T. L., Surratt, C. K., Lever, J. R., Acharya, R., Vaughan, R. A., Pandhare, A., and Blanton, M. P. (2012) (±)-2-(N-tert-Butylamino)-3′-[(125)I]-iodo-4′- azidopropiophenone: A dopamine transporter and nicotinic acetylcholine receptor photoaffinity ligand based on bupropion (Wellbutrin, Zyban) Bioorg. Med. Chem. Lett. 22, 523-526
13. Chiara, D. C., Dangott, L. J., Eckenhoff, R. G., and Cohen, J. B. (2003) Identification of nicotinic acetylcholine receptor amino acids photolabeled by the volatile anesthetic halothane Biochemistry 42, 13457-13467
14. Pedersen, S. E., Dreyer, E. B., and Cohen, J. B. (1986) Location of ligand-binding sites on the nicotinic acetylcholine receptor alpha-subunit J. Biol. Chem. 261, 13735-13743
15. Fong, T. M. and McNamee, M. G. (1986) Correlation between acetylcholine receptor function and structural properties of membranes Biochemistry 25, 830-840
16. Hamouda, A. K., Sanghvi, M., Sauls, D., Machu, T. K., and Blanton, M. P. (2006) Assessing the lipid requirements of the Torpedo californica nicotinic acetylcholine receptor Biochemistry 45, 4327-4337
17. Marsal, J., Tigyi, G., and Miledi, R. (1995) Incorporation of acetylcholine receptors and Cl- channels in Xenopus oocytes injected with Torpedo electroplaque membranes Proc. Natl. Acad. Sci. U. S. A. 92, 5224-5228
18. Morales, A., Aleu, J., Ivorra, I., Ferragut, J. A., Gonzalez-Ros, J. M., and Miledi, R. (1995) Incorporation of reconstituted acetylcholine receptors from Torpedo into the Xenopus oocyte membrane Proc. Natl. Acad. Sci. U. S. A. 92, 8468-8472
19. Moore, M. A. and McCarthy, M. P. (1995) Snake venom toxins, unlike smaller antagonists, appear to stabilize a resting state conformation of the nicotinic acetylcholine receptor Biochim. Biophys. Acta 1235, 336-342
20. Gallagher, M. J. and Cohen, J. B. (1999) Identification of amino acids of the torpedo nicotinic acetylcholine receptor contributing to the binding site for the noncompetitive antagonist [(3)H]tetracaine Mol. Pharmacol. 56, 300-307
21. Hamouda, A. K., Chiara, D. C., Blanton, M. P., and Cohen, J. B. (2008) Probing the structure of the affinity-purified and lipid-reconstituted torpedo nicotinic acetylcholine receptor Biochemistry 47, 12787-12794
22. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature 227, 680-685
23. Cleveland, D. W., Fischer, S. G., Kirschner, M. W., and Laemmli, U. K. (1977) Peptide mapping by limited proteolysis in sodium dodecyl sulfate and analysis by gel electrophoresis J. Biol. Chem. 252, 1102-1106
24. Schagger, H. and von Jagow, G. (1987) Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa Anal. Biochem. 166, 368-379
25. Blanton, M. P. and Cohen, J. B. (1994) Identifying the lipid-protein interface of the Torpedo nicotinic acetylcholine receptor: secondary structure implications Biochemistry 33, 2859-2872
26. Baenziger, J. E., Morris, M. L., Darsaut, T. E., and Ryan, S. E. (2000) Effect of membrane lipid composition on the conformational equilibria of the nicotinic acetylcholine receptor J. Biol. Chem. 275, 777-784
27. Blanton, M. P., Dangott, L. J., Raja, S. K., Lala, A. K., and Cohen, J. B. (1998) Probing the structure of the nicotinic acetylcholine receptor ion channel with the uncharged photoactivable compound -3H-diazofluorene J. Biol. Chem. 273, 8659-8668
28. Blanton, M. P., McCardy, E. A., Huggins, A., and Parikh, D. (1998) Probing the structure of the nicotinic acetylcholine receptor with the hydrophobic photoreactive probes [125I]TID-BE and [125I]TIDPC/16 Biochemistry 37, 14545-14555
29. Blanton, M. P., Li, Y. M., Stimson, E. R., Maggio, J. E., and Cohen, J. B. (1994) Agonist-induced photoincorporation of a p-benzoylphenylalanine derivative of substance P into membrane-spanning region 2 of the Torpedo nicotinic acetylcholine receptor delta subunit Mol. Pharmacol. 46, 1048-1055
30. Miyazawa, A., Fujiyoshi, Y., and Unwin, N. (2003) Structure and gating mechanism of the acetylcholine receptor pore Nature 423, 949-955
31. Blanton, M. P., Xie, Y., Dangott, L. J., and Cohen, J. B. (1999) The steroid promegestone is a noncompetitive antagonist of the Torpedo nicotinic acetylcholine receptor that interacts with the lipid-protein interface Mol. Pharmacol. 55, 269-278
32. Garcia, G., III, Chiara, D. C., Nirthanan, S., Hamouda, A. K., Stewart, D. S., and Cohen, J. B. (2007) [3H]Benzophenone photolabeling identifies state-dependent changes in nicotinic acetylcholine receptor structure Biochemistry 46, 10296-10307
33. White, B. H., Howard, S., Cohen, S. G., and Cohen, J. B. (1991) The hydrophobic photoreagent 3-(trifluoromethyl)-3-m-([125I] iodophenyl) diazirine is a novel noncompetitive antagonist of the nicotinic acetylcholine receptor J. Biol. Chem. 266, 21595-21607
34. White, B. H. and Cohen, J. B. (1992) Agonist-induced changes in the structure of the acetylcholine receptor M2 regions revealed by photoincorporation of an uncharged nicotinic noncompetitive antagonist J. Biol. Chem. 267, 15770-15783
35. Akabas, M. H. and Karlin, A. (1995) Identification of acetylcholine receptor channel-lining residues in the M1 segment of the alpha-subunit Biochemistry 34, 12496-12500
36. Yu, Y., Shi, L., and Karlin, A. (2003) Structural effects of quinacrine binding in the open channel of the acetylcholine receptor Proc. Natl. Acad. Sci. U. S. A. 100, 3907-3912
37. Nirthanan, S., Garcia, G., III, Chiara, D. C., Husain, S. S., and Cohen, J. B. (2008) Identification of binding sites in the nicotinic acetylcholine receptor for TDBzl-etomidate, a photoreactive positive allosteric effector J. Biol. Chem. 283, 22051-22062
38. Hamouda, A. K., Stewart, D. S., Husain, S. S., and Cohen, J. B. (2011) Multiple transmembrane binding sites for p-trifluoromethyldiazirinyl-etomidate, a photoreactive Torpedo nicotinic acetylcholine receptor allosteric inhibitor J. Biol. Chem. 286, 20466-20477
39. Arevalo, E., Chiara, D. C., Forman, S. A., Cohen, J. B., and Miller, K. W. (2005) Gating-enhanced accessibility of hydrophobic sites within the transmembrane region of the nicotinic acetylcholine receptor's {delta}-subunit. A time-resolved photolabeling study J. Biol. Chem. 280, 13631-13640
40. Yamodo, I. H., Chiara, D. C., Cohen, J. B., and Miller, K. W. (2010) Conformational changes in the nicotinic acetylcholine receptor during gating and desensitization Biochemistry 49, 156-165